This is a repository copy of The evolution of parental cooperation in birds.
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http://eprints.whiterose.ac.uk/94270/
Version: Accepted Version
Article:
Remes, V., Freckleton, R.P., Tokolyi, J. et al. (2 more authors) (2015) The evolution of
parental cooperation in birds. Proceedings of the National Academy of Sciences , 112 (44).
pp. 13603-13608. ISSN 1091-6490
https://doi.org/10.1073/pnas.1512599112
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Classification!
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Biological!Sciences,!Evolution!
2!
!
3!
Title
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The-evolution-of-parental-cooperation-in-birds
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-6!
Short-title!
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Parental!cooperation!in!birds!
8!
!
9!
Authors-10!
Vladimír-Remeš
a,-Robert-P.-Freckleton
b,-Jácint-Tökölyi
c,-András-Liker
d,-Tamás-Székely
e,f!
11!
!
12!
Author-affiliation!
13!
aDepartment!of!Zoology!and!Laboratory!of!Ornithology,!Palacky!University,!17.!listopadu!50,!77146!
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Olomouc,!Czech!Republic!
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bDepartment!of!Animal!and!Plant!Sciences,!Alfred!Denny!Building,!University!of!Sheffield,!Sheffield!S10!
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2TN,!UK!
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cMTATDE!“Lendület“!Behavioural!Ecology!Research!Group,!Department!of!Evolutionary!Zoology,!
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University!of!Debrecen,!Egyetemtér!1,!4032!Debrecen!
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dDepartment!of!Limnology,!University!of!Pannonia,!Wartha!Vince!u.!1.,!HT8201!Veszprém,!Hungary!
20!
eDepartment!of!Biology!and!Biochemistry,!University!of!Bath,!Bath!BA2!7AY,!UK!
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fState!Key!Laboratory!of!Biocontrol!and!College!of!Ecology!and!Evolution,!Sun!YatTsen!University,!
22!
Guangzhou!5102275,!China!
23!
!
24!
Corresponding-author!
25!
Vladimír!Remeš,!Department!of!Zoology!and!Laboratory!of!Ornithology,!Palacky!University,!17.listopadu!
26!
50,!77146!Olomouc,!Czech!Republic!
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tel:!+420T585634221!
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!
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Abstract!
31!
Parental!care!is!one!of!the!most!variable!social!behaviors!and!it!is!and!excellent!model!system!to!
32!
understand!cooperation!between!unrelated!individuals.!Three!major!hypotheses!have!been!proposed!to!
33!
explain!the!extent!of!parental!cooperation:!sexual!selection,!social!environment,!and!environmental!
34!
harshness.!Using!the!most!comprehensive!dataset!on!parental!care!that!includes!659!bird!species!from!
35!
113!families!covering!both!uniparental!and!biparental!taxa,!we!show!that!the!degree!of!parental!
36!
cooperation!is!associated!with!both!sexual!selection!and!social!environment.!Consistent!with!recent!
37!
theoretical!models!parental!cooperation!decreases!with!the!intensity!of!sexual!selection!and!with!skewed!
38!
adult!sex!ratios.!These!effects!are!additive!and!robust!to!the!influence!of!lifeThistory!variables.!However,!
39!
parental!cooperation!is!unrelated!to!environmental!factors!(measured!at!the!scale!of!whole!species!
40!
ranges)!as!indicated!by!a!lack!of!consistent!relationship!with!ambient!temperature,!rainfall!or!their!
41!
fluctuations!within!and!between!years.!These!results!highlight!the!significance!of!social!effects!for!
42!
parental!cooperation!and!suggest!that!several!parental!strategies!may!coTexist!in!a!given!set!of!ambient!
43!
environment.!
44!
!
45!
!
46!
Significance-Statement!
47!
Parents!in!many!animal!species!care!for!their!offspring.!In!some!species!males!care!more,!in!other!species!
48!
females!care!more,!whereas!in!still!other!species!the!contribution!of!the!sexes!is!equal.!Yet,!we!do!not!
49!
know!what!explains!these!differences!among!species.!Using!the!most!comprehensive!analyses!of!parental!
50!
care!to!date,!here!we!show!that!parents!cooperate!more!when!sexual!selection!is!not!intense!and!the!adult!
51!
sex!ratio!of!males!to!females!is!not!strongly!skewed.!However,!the!degree!of!parental!cooperation!is!
52!
unrelated!to!harshness!and!predictability!of!the!ambient!environment!during!the!breeding!season.!Our!
53!
work!therefore!suggests!that!several!types!of!parental!care!may!coTexist!in!a!given!set!of!ambient!
54!
environment.!
55!
Parental!cooperation,!defined!here!as!the!extent!of!biparental!care,!varies!along!a!continuum!from!
57!
approximately!equal!share!by!the!male!and!female!to!obligate!uniparental!care,!whereby!one!parent!(the!
58!
male!or!the!female)!provides!all!care!for!the!young!(1,!2).!By!cooperating!with!each!other,!the!male!and!the!
59!
female!parent!increase!growth!and!survival!of!their!young!in!various!insects,!fishes,!amphibians,!birds,!
60!
and!mammals!(3–5).!Thus!the!extent!of!parental!cooperation!may!influence!reproductive!success!and!
61!
population!dynamics.!Parental!care!is!an!excellent!model!system!for!investigating!interactions!between!
62!
two!unrelated!individuals!(6,!7),!and!it!is!one!of!the!prime!examples!of!gameTtheoretic!analyses!of!conflict!
63!
and!cooperation!both!theoretically!and!empirically!(8–11).!Therefore,!understanding!the!drivers!of!
64!
parental!cooperation!is!one!of!the!lynchpins!of!breeding!system!evolution!and!cooperative!behavior.!
65!
!
66!
Sexual!selection,!social!environment,!and!ambient!environment!have!been!proposed!to!explain!variation!
67!
in!the!extent!of!cooperation!between!parents!(7,!12–14).!First,!cooperation!between!parents!should!
68!
decrease!with!the!intensity!of!sexual!selection!(10,!15,!16)!and!a!reason!for!this!reduction!may!be!that!
69!
sexual!selection!favors!the!sex!with!higher!variance!in!mating!success!to!reduce!his!(or!her)!care!
70!
provisioning!(17–19).!Moreover,!high!mating!effort!might!further!decrease!the!ability!of!the!sex!under!
71!
stronger!sexual!selection!to!contribute!to!parental!care!(20).!Furthermore,!high!rates!of!extraTpair!
72!
paternity!should!lead!to!the!evolution!of!reduced!care!provisioning!by!males!(21–25).!This!evolutionary!
73!
reduction!of!paternal!care!in!species!with!high!extraTpair!paternity!would!translate!into!reduced!parental!
74!
cooperation.!Second,!the!sex!that!is!in!short!supply!in!the!population!has!an!increased!mating!opportunity!
75!
and!is!thus!less!likely!to!provide!care!than!the!more!abundant!sex!(26–28).!Therefore,!social!environment!
76!
(i.e.,!sex!ratio!of!adults!in!the!population)!is!expected!to!influence!parental!behavior!(8,!23,!29,!30).!Third,!
77!
environmental!factors!are!known!to!influence!complex!social!behavior!in!vertebrates!(31–33).!More!
78!
specifically,!demanding!environmental!conditions!imposing!higher!costs!of!living,!such!as!low!food!supply!
79!
or!harsh!and!unpredictable!climates,!should!promote!parental!cooperation!(34–36)!and!limit!social!
80!
conflict!(37),!and!this!idea!has!been!recently!backed!by!extensive!modeling!(38–39).!Although!previous!
81!
tests!of!these!hypotheses!provided!important!insights!into!the!potential!drivers!of!parental!cooperation,!
82!
no!study!has!yet!tested!all!three!hypotheses!across!a!broad!range!of!taxa!and!assessed!their!relative!
83!
importance.!
84!
!
85!
Here,!we!use!data!on!parental!cooperation!in!659!bird!species!from!113!families!to!test!these!three!major!
86!
hypotheses.!Birds!are!one!of!the!most!suitable!organisms!to!test!these!propositions,!since!they!exhibit!the!
87!
on!parental!behavior!of!a!broad!range!of!taxa!from!wild!populations.!Since!parental!care!is!a!complex!trait,!
89!
we!compiled!data!on!8!components!of!care!(40)!and!quantified!parental!cooperation!based!on!sexTspecific!
90!
contribution!to!care!in!these!parental!activities!spanning!the!whole!parental!care!period!(full!Materials!
91!
and!Methods!are!available!in!SI!Appendix,!Supplement!S1).!We!focused!on!care!provisioning!by!the!male!
92!
and!the!female!parent,!and!the!extent!of!parental!cooperation!was!estimated!on!a!scale!that!varied!
93!
between!−1.5!when!only!one!parent!(the!male!or!the!female)!provides!all!care!and!1.5!when!the!male!and!
94!
the!female!parent!share!provisioning!approximately!equally!(frequency!distribution!of!parental!
95!
cooperation!across!659!species!of!birds!is!available!in!SI!Appendix,!Fig.!S1).!
96!
!
97!
Using!phylogenetic!analyses!we!test!the!following!predictions:!i)!sexual!selection:!parental!cooperation!is!
98!
higher!in!socially!monogamous!species!and!in!species!with!low!rates!of!extraTpair!paternity!(EPP),!than!in!
99!
polygamous!and!high!EPP!species,!respectively;!ii)!social!environment:!species!with!balanced!adult!sex!
100!
ratios!(ASR,!proportion!of!males!in!the!adult!population)!exhibit!more!parental!cooperation!than!species!
101!
with!biased!ASR;!and!iii)!ambient!environment:!species!that!live!in!environments!with!harsh!and!variable!
102!
climates!exhibit!high!parental!cooperation.!
103!
!
104!
Results-and-Discussion!
105!
The!extent!of!parental!cooperation!is!usually!conserved!within!major!clades!(Fig.!1),!which!is!consistent!
106!
with!high!values!of!phylogenetic!signal!(λ ≈!0.9,!Table!1;!exact!estimated!λ!values!are!available!in!SI!
107!
Appendix,!Table!S1).!At!the!same!time,!parental!cooperation!is!highly!variable!between!clades!across!
108!
birds.!For!example,!grebes,!woodpeckers,!and!sparrows!are!characterized!by!extensive!parental!
109!
cooperation,!whereas!others!exhibit!low!cooperation!(e.g.!ducks,!pheasants!and!grouse,!and!owls,!Fig!1).!
110!
Several!clades,!however,!exhibit!high!interTspecific!variation!in!parental!cooperation;!for!example!snipes,!
111!
sandpipers!and!allies,!and!Old!World!warblers!(Fig.!1).!
112!
!
113!
Both!sexual!selection!and!social!environment!predict!parental!cooperation!as!shown!by!phylogenetic!
114!
generalized!least!squares!analyses!(41)!using!the!most!recent!complete!avian!phylogeny!(42)!(Table!1,!
115!
Figs.!2,!3;!for!details!of!these!relationships!see!SI!Appendix,!Table!S1!and!Fig.!S2).!First,!intense!sexual!
116!
selection!as!indicated!by!extensive!sexual!size!dimorphism!(43)!and!high!rates!of!extraTpair!paternity!are!
117!
consistently!associated!with!low!parental!cooperation!(Figs.!2,!3).!To!confirm!that!our!predictions!also!
118!
hold!when!testing!the!male!involvement!in!care,!we!also!analyzed!relative!male!care,!which!is!a!proxy!of!
119!
of!relative!male!care!across!659!species!of!birds!is!available!in!SI!Appendix,!Fig.!S1).!Our!predictions!are!
121!
supported,!since!male!care!(relative!to!female!care)!is!low!in!species!with!maleTbiased!sexual!size!
122!
dimorphism!and!high!in!species!with!femaleTbiased!dimorphism.!Moreover,!males!provide!little!care!in!
123!
species!with!high!extraTpair!paternity!(Fig.!3;!summarized!results!are!available!in!SI!Appendix,!Table!S2!
124!
while!detailed!results!are!available!in!SI!Appendix,!Table!S3!and!Fig.!S3).!
125!
!
126!
These!results!are!in!line!with!theories!of!the!evolution!of!parental!cooperation!(2,!17,!25,!44).!Specifically,!
127!
our!results!are!consistent!with!the!prediction!that!the!larger!sex!(usually!the!male!in!birds),!which!is!often!
128!
under!stronger!sexual!selection!than!the!smaller!sex,!reduces!its!care!provisioning!(17,!19),!translating!
129!
into!lower!contribution!to!care!on!macroevolutionary!timescales.!Similarly,!our!results!support!the!
130!
prediction!that!high!rates!of!extraTpair!paternity!will!lead,!on!a!macroevolutionary!timescale,!to!a!
131!
reduction!in!male!care!(22–25)!and!consequently!to!reduced!parental!cooperation.!At!the!same!time,!this!
132!
result!is!far!from!trivial,!because!some!models!predict!variable!relationships!between!male!care!and!extraT
133!
pair!paternity!depending!on!model!assumptions!(45)!and!results!of!previous!empirical!studies!are!also!
134!
conflicting!(e.g.!22,!46–48,!reviewed!in!25).!It!is!worth!stressing!that!the!relationship!we!document!is!the!
135!
most!comprehensive!in!any!major!taxon!and!makes!a!significant!contribution!to!previous!theoretical!and!
136!
empirical!investigations!of!extraTpair!paternity!and!parental!care.!The!macroevolutionary!response!of!
137!
male!care!to!extraTpair!paternity!may!not!depend!on!the!ability!of!males!to!perceive!paternity!loss!in!their!
138!
contemporary!broods!and!respond!to!it!by!facultative!reduction!of!paternal!care!(21,!22,!24,!46),!although!
139!
this!ability!seems!to!be!widespread!among!animals!(25).!Reduction!of!male!parental!contribution!due!to!
140!
female!promiscuity!might!lead!to!lower!overall!parental!effort!(49),!and!eventual!breakdown!of!biparental!
141!
breeding!systems!(21).!
142!
!
143!
Second,!parental!cooperation!decreases!with!biased!adult!sex!ratios!(Table!1,!Figs.!2,!3).!This!result!is!in!
144!
line!with!theoretical!prediction!that!biased!sex!ratios!will!promote!divergent!parental!sex!roles,!because!
145!
individuals!of!the!rare!sex!reduce!their!care!due!to!high!mating!success,!while!members!of!the!more!
146!
common!sex!get!most!reproductive!success!from!caring!for!existing!offspring!(8,!23).!This!interpretation!is!
147!
supported!by!modeling!of!relative!male!care,!which!is!low!in!species!with!femaleTbiased!sex!ratio!and!high!
148!
in!species!with!maleTbiased!sex!ratio!(Fig.!3;!summarized!results!are!available!in!SI!Appendix,!Table!S2!
149!
while!detailed!results!are!available!in!SI!Appendix,!Table!S3!and!Fig.!S3).!Our!results!are!also!in!line!with!
150!
previous!findings!in!shorebirds,!where!ASR!strongly!predicted!conventional!and!reversed!parental!sex!
151!
causality!might!be!reversed.!Unequal!parental!roles!might!lead!to!biased!sex!ratios!because!the!sexes!
153!
engage!unequally!in!parental!duties,!have!different!time!budgets,!and!consequently!experience!different!
154!
mortality!rates!(50).!Accordingly,!sexTbiased!mortality!rates!are!often!correlated!with!biased!ASR!across!
155!
populations!and!species!(51–53).!Moreover,!some!authors!suggest!positive!feedbacks!between!changes!in!
156!
ASR!and!parental!sex!roles!and!thus!the!relationship!may!even!be!bidirectional!(8,!23,!54).!
157!
!
158!
The!aforementioned!results!are!not!confounded!by!phylogeny!since!we!use!phylogenyTbased!comparative!
159!
analyses,!and!remain!robust!to!alternative!phylogenetic!hypotheses!and!incorporating!potential!
160!
confounds!in!the!models!(for!phylogenetic!robustness!of!our!results!see!SI!Appendix,!Tables!S1!and!S3).!In!
161!
addition!to!sexual!selection!and!social!environment,!we!find!a!positive!relationship!of!parental!
162!
cooperation!to!adult!body!mass,!although!this!effect!is!less!consistent!between!analyses!(Table!1,!Fig.!3).!
163!
Body!mass!is!a!typical!allometric!correlate!of!life!history,!including!breeding!cycle!duration!(for!the!
164!
relationship!of!breeding!cycle!duration!to!adult!body!mass!in!our!dataset!see!SI!Appendix,!Fig.!S4)!and!
165!
adult!mortality!rate!(correlation!in!our!dataset!r!=!−0.57,!n!=!323!species),!and!of!pair!bond!duration!and!
166!
divorce!rate!(55,!56).!Consequently,!it!seems!that!longTlived!species!with!prolonged!pair!bonds!and!low!
167!
divorce!rates!would!be!expected!to!cooperate!more,!but!more!direct!tests!of!this!hypothesis!are!needed.!
168!
We!find!that!chick!development!(altricial!vs.!precocial)!is!not!associated!with!the!extent!of!cooperation!or!
169!
relative!male!care!(Table!1,!Fig.!3),!suggesting!that!chick!demand!does!not!affect!parental!cooperation!
170!
strategies!across!birds.!We!highlight!that!sexual!selection!and!social!environment!together!with!body!
171!
mass!explain!a!large!proportion!of!variance!in!parental!cooperation!(approx.!30T35%;!summary!in!Table!1!
172!
and!details!in!SI!Appendix,!Table!S1),!although!these!values!are!somewhat!lower!for!relative!male!care!
173!
(approx.!12T26%;!summary!in!SI!Appendix,!Table!S2!and!details!in!SI!Appendix,!Table!S3).!We!also!
174!
emphasize!that!recent!work!suggests!that!ASR!relates!to!sexual!selection!(57)!and!the!precise!relationship!
175!
between!ASR,!demographic!processes,!and!sexual!selection!are!far!from!understood!(53).!Nevertheless,!
176!
our!results!demonstrate!large!additive!effects!of!major!selective!forces!that!were!theoretically!predicted!
177!
to!facilitate!parental!cooperation!in!animals.!
178!
!
179!
Finally,!climatic!conditions!during!the!breeding!season,!thought!to!drive!the!evolution!of!cooperation!(33,!
180!
34,!58),!do!not!predict!parental!cooperation!as!none!of!the!climatic!factors!is!significantly!associated!with!
181!
parental!cooperation!either!in!bivariate!or!multiple!regression!analyses!(Table!1,!Fig.!3;!for!details!of!these!
182!
relationships!see!SI!Appendix,!Table!S1!and!Fig.!S2).!Our!analyses!thus!suggest!that!climatic!conditions!
183!
cooperation!strategies.!This!conclusion!agrees!with!observations!that!species!with!extremely!contrasting!
185!
parental!care!systems!(e.g.!with!reversed!vs.!conventional!sex!roles)!may!breed!sideTbyTside!sharing!much!
186!
of!the!environment!(see!ref.!27!for!examples).!Weak!or!inconsistent!effects!of!climate!have!previously!
187!
been!identified!in!largeTscale!analyses!of!climatic!correlates!of!cooperative!breeding!and!sexual!size!
188!
dimorphism!in!birds!(34,!58–60).!Taken!together!with!our!new!results!presented!here,!this!body!of!work!
189!
suggests!that!sexual,!social,!and!parenting!strategies!in!birds!are!largely!independent!of!climatic!effects!on!
190!
the!scale!of!whole!breeding!ranges!of!species!and!instead!might!be!driven!by!ecoTevolutionary!feedbacks!
191!
between!social!behavior,!life!history,!and!demography!(29,!61).!It!is!also!possible!that!parental!
192!
cooperation!may!covary!with!environmental!factors!at!finer!spatial!scales!not!captured!by!our!analyses!of!
193!
breeding!rangeTwide!environment,!for!example!as!seems!to!be!the!case!of!mating!systems!and!sexual!
194!
selection!(31,!32,!35,!60).!We!suggest!that!detailed!analyses!of!the!plasticity!of!parental!cooperation!
195!
within!species!in!relation!to!environmental!conditions!on!smaller!spatial!scales!(e.g.!food!supply,!ambient!
196!
temperature)!will!shed!critical!light!on!this!important!question.!
197!
!
198!
In!conclusion,!we!show!that!the!evolution!of!parental!cooperation!is!predicted!by!sexual!selection!and!
199!
social!environment!at!least!in!birds,!whereas!climatic!conditions!at!the!scale!of!the!whole!species’!
200!
breeding!ranges!do!not!predict!parental!cooperation.!Thus,!several!parental!cooperation!strategies!may!be!
201!
adaptive!in!a!given!set!of!climatic!conditions,!depending!on!the!species'!social!and!genetic!mating!systems!
202!
and!demographic!structure.!These!patterns!are!valid!across!a!broad!range!of!bird!species!and!clades!that!
203!
breed!in!diverse!settings.!They!highlight!the!significance!of!feedbacks!between!sexual!selection,!social!
204!
environment,!and!parental!care,!since!all!of!these!have!mortality!consequences!and!are!thus!linked!in!ecoT
205!
evolutionary!feedback!loops!(61).!
206!
!
207!
Further!works!are!needed!to!advance!parental!cooperation!research.!First,!drivers!of!the!effects!we!
208!
identify!are!sometimes!unclear.!For!example,!it!is!not!clear!whether!evolutionary!changes!in!parental!
209!
cooperation!are!driven!by!sexual!selection!acting!on!male!behavior!(24,!46),!on!female!behavior!(62)!or!on!
210!
both!sexes!simultaneously.!Second,!further!studies!should!explore!which!sex!is!more!responsive!and!
211!
whether!sexTspecific!parenting!abilities!can!bias!responses!to!intense!sexual!selection!(10,!11).!Third,!new!
212!
phylogenetic!comparative!analyses!are!needed!to!test!whether!sexual!selection!and!social!environment!
213!
may!influence!parental!cooperation!in!nonTavian!taxa,!for!instance!in!fishes,!frogs,!and!mammals.!Whilst!
214!
the!details!of!care!differ!between!these!major!clades,!our!results!here!establish!the!working!hypotheses!
215!
have!important!effects!on!parental!cooperation.!For!example,!food!availability!predicts!cooperation!during!
217!
nestling!feeding!in!several!avian!groups!(35,!36),!and!the!generality!of!this!relationship!should!be!tested!
218!
using!largeTscale!data!sets.!Moreover,!our!rangeTwide!analyses!might!have!missed!the!importance!of!
219!
ecological!factors!operating!on!smaller!spatial!scales.!We!encourage!researchers!to!evaluate!potential!
220!
effects!of!smallTscale!ecological!factors!on!parental!cooperation.!Finally,!insights!gained!by!our!
221!
comparative!study!should!be!further!tested!in!the!natural!habitat!of!animals.!These!fieldTbased!
222!
observations!and!experimental!manipulations!combined!with!comparisons!across!populations!and!longT
223!
term!population!monitoring!data!will!be!immensely!useful!to!tease!apart!various!social!and!ecological!
224!
effects!and!allow!evolutionary!ecologists!to!test!the!positive!and!negative!feedbacks!that!underpin!mating!
225!
systems!and!parental!care.!
226!
!
227!
Materials-and-Methods!
228!
Data!collection!
229!
We!quantified!sexTspecific!contribution!to!care!on!an!ordinal!scale!from!0!to!4!as!follows:!0!T!no!male!
230!
contribution,!1!T!male!contribution!1T33%,!2!T!male!contribution!34T66%,!3!T!male!contribution!67T99%,!4!
231!
T!male!contribution!100%.!Thus,!this!score!varied!from!femaleTonly!care!(0)!to!approximately!equal!care!
232!
by!male!and!female!(2)!to!maleTonly!care!(4).!Scores!were!gathered!separately!for!nest!building,!
233!
incubation,!nest!guarding!(i.e.,!guarding!and!defending!the!nest!during!incubation),!chick!brooding,!chick!
234!
feeding,!chick!guarding!(i.e.,!guarding!and!defending!the!brood!after!hatching),!postTfledging!feeding!of!
235!
chicks,!and!postTfledging!guarding!of!chicks!(i.e.,!guarding!and!defending!the!brood!after!fledging,!for!
236!
details!see!ref.!40).!To!represent!the!extent!of!biparental!care,!the!eight!parental!activities!were!reTcoded!
237!
on!a!3!level!scale!so!that!0!represented!exclusive!uniparental!care!by!the!male!or!female!(original!scores!0!
238!
or!4),!1!represented!biparental!care!biased!toward!either!the!male!or!the!female!(original!scores!1!or!3),!
239!
and!2!represented!approximately!equal!contribution!by!the!male!and!female!(original!score!2).!Finally,!we!
240!
calculated!parental!cooperation!by!averaging!the!statistically!centered!extent!of!biparental!care!across!the!
241!
eight!activities.!The!resulting!parental!cooperation!ranged!from!minimum!parental!cooperation!to!
242!
maximum!parental!cooperation!(frequency!distribution!of!parental!cooperation!across!659!species!of!
243!
birds!is!available!in!SI!Appendix,!Fig.!S1)!and!varied!across!the!phylogeny!(Fig.!1).!Here,!minimum!
244!
cooperation!is!when!all!activities!are!carried!out!by!one!sex!(the!male!or!the!female,!ca.!around!the!value!
245!
of!−1.5),!whereas!the!maximum!cooperation!is!when!all!parental!care!activities!are!shared!approximately!
246!
equally!between!the!male!and!the!female!(ca.!around!the!value!of!1.5).!To!test!hypotheses!that!predict!
247!
standardized!relative!male!care!based!on!the!original!scores.!Relative!male!care!ranged!from!−2!(strongly!
249!
femaleTbiased!care)!to!3!(strongly!maleTbiased!care;!frequency!distribution!of!relative!male!care!across!
250!
659!species!of!birds!is!available!in!SI!Appendix,!Fig.!S1).!Data!collection!was!designed!to!cover!the!broad!
251!
phylogenetic!diversity!and!full!variability!of!breeding!systems!exhibited!by!birds.!Our!data!set!contained!
252!
659!species!from!113!avian!families.!
253!
!
254!
We!used!two!proxies!of!sexual!selection!that!are!widely!available:!sexual!size!dimorphism!and!extraTpair!
255!
paternity!(63).!We!note!that!the!relationship!between!the!strength!of!sexual!selection!and!EPP!is!complex.!
256!
However,!by!using!several!indices!of!sexual!selection!(sexual!size!dimorphism,!EPP)!we!hope!to!provide!
257!
comprehensive!analyses!and!characterize!broad!range!of!processes!that!underpin!sexual!selection,!
258!
including!maleTmale!competition!and!female!choice.!We!calculated!size!dimorphism!index!as!SDI!=!body!
259!
mass!of!the!heavier!sex!divided!by!body!mass!of!the!lighter!sex!minus!one!and!made!the!values!positive!
260!
for!maleTbiased!dimorphism!and!negative!for!femaleTbiased!dimorphism.!We!then!also!calculated!absolute!
261!
SDI!by!taking!absolute!values!of!the!original!SDI.!Greater!values!of!absolute!SDI!thus!mean!greater!
262!
difference!in!body!masses!between!sexes,!suggesting!differential!selection!acting!on!males!and!females!
263!
that!may!indicate!sexual!selection!(15,!43).!ExtraTpair!paternity!(EPP)!was!expressed!as!%!of!broods!
264!
containing!at!least!one!extraTpair!offspring,!in!accordance!with!recent!studies!(64).!However,!to!check!the!
265!
sensitivity!of!our!analyses!to!this!particular!choice,!we!also!repeated!all!analyses!with!%!of!extraTpair!
266!
offspring!in!the!population!(EPY).!Although!this!variable!strongly!decreased!sample!size,!results!were!
267!
largely!robust!to!the!choice!of!EPP!vs.!EPY!(details!of!these!sensitivity!analyses!are!available!in!SI!
268!
Appendix,!Tables!S1!and!S3).!Social!environment!was!characterized!by!adult!sex!ratio!(ASR),!which!was!
269!
expressed!as!the!proportion!of!males!in!the!adult!population!(52,!65).!We!then!calculated!the!absolute!
270!
deviation!from!ASR!of!0.5!to!express!the!degree!of!bias!in!the!frequency!of!males!vs.!females!in!the!
271!
population.!This!value!was!always!positive!and!increased!with!increasing!deviation!from!ASR!of!0.5!(ASR!
272!
bias).!
273!
!
274!
To!characterize!ambient!environment,!first!we!recorded!breeding!season!for!each!species!from!literature.!
275!
Second,!based!on!digitized!ranges!(66)!and!global!climatic!layers!(CRU!Dataset,!
276!
http://www.cru.uea.ac.uk/),!we!extracted!climatic!conditions!in!the!breeding!range!of!every!species!
277!
during!its!breeding!season.!We!extracted!i)!the!average!monthly!temperature!(∘C)!and!rainfall!(mm);!ii)!
278!
withinTyear!variation!as!SD!of!breeding!season!monthly!averages!for!temperature!and!rainfall;!and!iii)!
279!
amongTyear!variation!as!SD!across!49!years!(1961T2009)!of!monthly!averages!for!temperature!and!
rainfall!during!the!species'!breeding!season.!To!control!for!potential!lifeThistory!confounds,!we!included!
281!
adult!body!mass!(g)!and!chick!development!(altricial!vs.!precocial)!in!the!models.!
282!
!
283!
Phylogenetic!analyses!
284!
We!used!phylogenetic!generalized!least!squares!(PGLS)!approach!implemented!in!a!fast!likelihood!
285!
algorithm!(67)!in!the!R!language!(68).!In!PGLS!models,!we!estimated!the!phylogenetic!signal!by!optimizing!
286!
the!λ!parameter!(41).!We!used!500!phylogenetic!trees!extracted!from!www.birdtree.org!(Hackett!
287!
constraint,!ref.!42).!We!ran!the!PGLS!analyses!across!all!the!trees!and!then!summarized!the!resulting!500!
288!
parameter!estimates.!
289!
!
290!
Parental!cooperation!and!relative!male!care!were!the!main!response!variables!in!our!models.!First,!we!
291!
fitted!bivariate!PGLS!models!between!parental!cooperation!and!the!following!predictors:!sexual!size!
292!
dimorphism!(log!absolute!SDI),!extraTpair!paternity!(sqrt!EPP),!adult!sex!ratio!(sqrt!ASR!bias),!climatic!
293!
variables!(means!and!amongT!and!withinTyear!variations!in!temperature!and!rainfall),!adult!body!mass!
294!
(logTtransformed),!and!chick!development!(altricial!vs.!precocial).!Predictors!were!the!same!for!relative!
295!
male!care,!except!that!we!used!SDI!instead!of!absolute!SDI,!ASR!instead!of!ASR!bias,!and!we!did!not!use!
296!
climatic!variables!due!to!lacking!predictions!for!relative!male!care.!Second,!we!fitted!PGLS!models!with!
297!
several!explanatory!variables.!To!use!the!maximum!number!of!species!in!each!analysis,!we!fitted!four!
298!
models!structured!according!to!our!three!main!hypotheses!while!controlling!for!lifeThistory!variables.!For!
299!
parental!cooperation,!these!were:!Sexual!selection!model!–!absolute!SDI,!EPP,!adult!body!mass,!chick!
300!
development!(n!=!226!species);!Social!environment!model!–!ASR!bias,!adult!body!mass,!chick!development!
301!
(n!=!165!species);!Climate!model!–!ambient!temperature,!rainfall,!adult!body!mass,!chick!development!(n!
302!
=!659!species);!Full!model!–!absolute!SDI,!EPP,!ASR!bias,!ambient!temperature,!rainfall,!adult!body!mass,!
303!
chick!development!(n!=!80!species).!For!relative!male!care,!these!were:!Sexual!selection!model!–!SDI,!EPP,!
304!
adult!body!mass,!chick!development!(n!=!226!species);!Social!environment!model!–ASR,!adult!body!mass,!
305!
chick!development!(n!=!165!species);!Full!model!–!SDI,!EPP,!ASR,!adult!body!mass,!chick!development!(n!=!
306!
80!species).!We!did!not!fit!the!climatic!model!due!to!lacking!predictions!for!relative!male!care.!Full!details!
307!
of!Materials!and!Methods!are!available!in!SI!Appendix,!Supplement!S1.!
308!
!
309!
Acknowledgments!
310!
We!appreciate!tremendous!work!of!generations!of!field!ornithologists.!This!work!would!not!be!possible!
311!
University!(IGA!PrF_2015_011).!A.L.!was!supported!by!a!Marie!Curie!IntraTEuropean!Fellowship,!and!by!
313!
the!grants!OTKA!K!112838!and!TÁMOPT4.2.2.BT15/1/KONVT2015T0004.!T.S.!was!a!Mercator!Visiting!
314!
Professor!at!the!University!of!Bielefeld,!and!a!Humboldt!Award!holder!at!the!University!of!Göttingen!
315!
whilst!working!on!this!paper,!and!was!supported!by!an!open!project!of!State!Key!Laboratory!of!Biocontrol,!
316!
Sun!YatTsen!University,!Guangzhou.!!J.T.!was!supported!by!TÁMOPT4.2.2.CT11/1/KONVT2012T0010!
317!
project,!coTfinanced!by!the!European!Social!Fund!and!the!European!Regional!Development!Fund.!
318!
!
319!
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320!
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males!in!response!to!selection!on!paternity!assurance!behaviour.!Ecol$Lett!17(7):803–810.!
63.!Dunn!PO,!Whittingham!LA,!Pitcher!TE!(2001)!Mating!systems,!sperm!competition,!and!the!evolution!of!
sexual!dimorphism!in!birds.!Evolution!55(1):161–75.!
64.!Cornwallis!CK,!West!SA,!Davis!KE,!Griffin!AS!(2010)!Promiscuity!and!the!evolutionary!transition!to!
complex!societies.!Nature!466(7309):969–972.!
65.!Donald!PF!(2007)!Adult!sex!ratios!in!wild!bird!populations.!Ibis$149(4):671–692.!
66.!BirdLifeTInternational,!NatureServe!(2011)!Bird$Species$Distribution$Maps$of$the$World!(Cambridge!
and!Arlington).!
67.!Freckleton!RP!(2012)!Fast!likelihood!calculations!for!comparative!analyses.!Methods$Ecol$Evol!
3(5):940–947.!
Figure-legends!
Fig.!1.!Phylogenetic!distribution!of!parental!cooperation!in!659!species!of!birds!included!in!this!study! (Bayesian!maximum!credibility!tree!of!500!phylogenies).!The!figure!shows!parental!cooperation!for!each! species!(black!bars!refer!to!parental!cooperation;!tall!bars!indicate!high!cooperation)!and!phylogenetic! reconstruction!along!the!branches!(using!plotBranchbyTrait!{phytools}!function!of!R!software;!red!=!high! cooperation,!yellow!=!low!cooperation).!
!
Fig.!2.!Parental!cooperation!in!relation!to!sexual!size!dimorphism!(log!absolute!Sexual!Dimorphism!Index),! extraTpair!paternity!(sqrt!EPP),!and!adult!sex!ratio!(sqrt!ASR!bias)!in!birds.!Variables!in!each!panel!were! statistically!adjusted!for!other!predictors!in!a!phylogenetic!generalized!least!squares!(PGLS)!model!and! the!residuals!from!statistical!models!are!plotted!(Sexual!selection!model!for!Sexual!size!dimorphism!and! ExtraTpair!paternity,!and!Social!environment!model!for!Adult!sex!ratio,!see!Table!1).!Ordinary!least! squares!regression!lines!are!included.!
!
Fig.!3.!Parental!cooperation!and!relative!male!care!(for!their!frequency!distribution!across!659!species!of! birds!see!SI!Appendix,!Fig.!S1)!in!relation!to!sexual!selection!(orange),!social!environment!(red),!climate! (green),!and!lifeThistory!traits!(pink).!The!figure!shows!effect!sizes!(mean!standardized!regression! coefficients!±!2SE)!from!the!phylogenetic!generalized!least!squares!analyses!of!parental!cooperation!and! relative!male!care.!Models!were!either!bivariate!(circles)!or!multiple!regressions!(other!symbols).!Multiple! regression!models!parallel!our!hypotheses:!sexual!selection!model!(squares),!social!environment!model! (diamonds),!climate!model!(upward!facing!triangles),!and!full!model!(downward!facing!triangles;!see!also! Table!1).!In!analyses!of!parental!cooperation,!we!used!absolute!SDI!and!ASR!bias,!whereas!in!analyses!of! relative!male!care,!we!used!SDI!and!ASR!(see!Materials!and!Methods!and!SI!Appendix,!Supplement!S1).! LifeThistory!covariates!(body!mass,!chick!development)!were!included!in!all!models.!Horizontal!error!bars! not!intercepting!the!vertical!zero!line!indicate!statistically!significant!effects.!Note!that!climate!was!not! fitted!in!models!of!relative!male!care.!
!
!
Table&1!!Parental(cooperation(in(relation(to(sexual(selection,(social(environment,(and(climate(in(
birds.'In'all'models'parental'cooperation'was'the'response'variable'and'predictors'included:'sexual'
size%dimorphism%(log%absolute%Size%Dimorphism%Index),%extra!pair%paternity((sqrt(EPP),(adult(sex(
ratio&(sqrt&ASR&bias),&temperature&(first&axis&from&PCA&on&climatic&variables:&higher&values&mean&hot&
environments*with$low$temperature$variability;!factor'loadings'available'in'SI#Appendix,#Table&S!),#
rainfall'(second'axis'from$PCA$on$climatic$variables:$higher$values$mean$dry$environments!with%high% rainfall'variability;'factor'loadings'available'in'SI#Appendix,!Table&S4),#body#mass#(log!
transformed),-and$chick$development$(altricial$vs.$precocial).$We$use$phylogenetic$generalized&least&squares&
approach'and'present'means'from'500'analyses'using'different'phylogenetic'trees'(see'detailed'
results'in'SI#Appendix,#Table&S1).&Estimates&are&standardized®ression&coefficients&and&λ"indicates)
the$strength%of%the%phylogenetic%signal!"
"
Model&and&predictors" Estimate((SE)" F"(P)
"
Sexual'selection'(R!!="0.17,"λ"="
0.76,&df&=&4,221)" " "
Sexual'size'dimorphism" !0.258&(0.057)" 20.62%(<0.001)
"
Extra!pair%paternity" !0.264&(0.061)" 18.55%(<0.001)
"
Body%mass" 0.299%(0.115)" 6.83%(0.011)
"
Chick&development" !0.157&(0.151)" 1.12$(0.308)
"
" " "
Social'environment'(R!!="0.07,"
!!="0.91,"df"="3,161)" " "
Adult&sex&ratio" !0.186&(0.056)" 11.05%(0.001)
"
Body%mass" 0.087%(0.135)" 0.43%(0.524)
"
Chick&development" !0.084%(0.261)" 0.12%(0.750)
"
" " "
Climate((R!!="0.01,"λ"="0.90,"df#
="4,654)" " "
Temperature" 0.041%(0.033)" 1.60%(0.214)
"
Rainfall" 0.037%(0.031)" 1.47%(0.233)
"
Body%mass" !0.019%(0.074)" 0.09$(0.795)
"
Chick&development" !0.084%(0.145)" 0.35%(0.564)
"
Full$model$(R!!="0.29,"λ"="0.82,"
df#=#7,72)" " "
Sexual'size%dimorphism" !0.168&(0.098)" 2.93%(0.093)
"
Extra!pair%paternity" !0.230%(0.106)" 4.70%(0.034)
"
Adult&sex&ratio" !0.234&(0.083)" 7.88$(0.007)
"
Temperature" 0.027%(0.105)" 0.08$(0.796)
"
Rainfall" 0.034%(0.087)" 0.16%(0.696)
"
Body%mass" 0.334%(0.178)" 3.54%(0.066)
"
Chick&development" 0.020$(0.223)" 0.03$(0.900)
"
"
Ratites
Gees & Swans
Ducks
Me gap
ode s, Q
uail & a llies
Ph
easa
nts, G
ro use & allies Sa nd gro use & G re bes St orks , H ero ns & allie s C uck oo s & Bu st ard s C ran es & R a ils N igh tja rs , H u mmi ng b ird Pl o ve rs , St ilt s & a llie Gu lls, Te rns & a
llie s
Ja ca
na s &
alli es
Sn ipe
s, Sa nd
pip ers
& a llie
s
Vultu res,
Haw ks &
Eagl es
Owls
Wood hoop
oes & Hornb
ills
Bee− eaters
& Kingf ishers
Barbets & Touca
ns
Woodpe ckers
Falcons
Parrots
Antbirds, Cotingas & Manakins Tyrant−flycatchers
Bowerbirds & Austr. TreecreepersFairy−wrens
Honeyeaters &
Thornbills Austr. Ba
bblers
& Logrunne rs Cro
ws, Vi reos
& allies
Au stra
lasi an R
ob ins Tits &
Chicka dees La rks Sw allow s & Ma rtins O ld W W arb lers & a llies W re ns & a llies St a rlin g s , Th ra sh e rs & a llies T h rush e
s & Flyca tch e rs Su nb ird s Wa xb ills & W
ea ve rs Sp arro ws Pipi ts &
Wag tails
Finch es
& H oneycre
epers
Card inal
s & Tana
gers
Wood Warb
lers
NW Bla ckbirds
2
1
0
1
1.0 0.5 0.0 0.5 1.0 1.5
Se
xu
a
l si
ze
d
imo
Parental cooperation
4
2
0
2
1.0 0.5 0.0 0.5 1.0 1.5
Ext
ra
p
a
ir
p
a
te
Parental cooperation
0
.3
0
.2
0
.1
0
.0
0
.1
1.5 1.0 0.5 0.0 0.5 1.0
Ad
u
lt
se
x
ra
tio
Chick development
Body mass
Rainfall
Ambient temperature
Adult sex ratio
Extra
−
pair paternity
Sexual size dimorphism
Supporting Information for:
The evolution of parental cooperation in birds
Authors
Vladimír Remeš, Robert P. Freckleton, Jácint Tökölyi, András Liker, Tamás Székely
Supplement S1. Full Materials and Methods.
Fig. S1. Frequency distribution of parental cooperation and relative male care in birds.
Fig. S2. Scatterplots of parental cooperation in relation to predictors as modeled by PGLS multiple
regressions.
Fig. S3. Scatterplots of relative male care in relation to predictors as modeled by PGLS multiple
regressions.
Fig. S4. Scatterplots of the durations of different phases of breeding cycle (nest building, egg incubation,
chick care before and after fledging) in relation to adult body mass.
Fig. S5. Estimates of semivariograms and Moran’s I for residuals from i) the four PGLS models of parental
cooperation with EPP, and ii) the three PGLS models of relative male care with EPP.
Table S1. Full results of PGLS models of parental cooperation run across 500 phylogenies.
Table S2. Summary of results of PGLS models of relative male care.
Table S3. Full results of PGLS models of relative male care run across 500 phylogenies.
Supporting Information for:
The evolution of parental cooperation in birds
Authors
Vladimír Remeš, Robert P. Freckleton, Jácint Tökölyi, András Liker, Tamás Székely
Supplement S1
Full Materials and Methods
Data collection
We quantified sex-specific contribution to care on an ordinal scale from 0 to 4 as follows: 0 - no male
contribution, 1 - male contribution 1-33%, 2 - male contribution 34-66%, 3 - male contribution 67-99%, 4
- male contribution 100%. Thus, this score varied from female-only care (0) to approximately equal care
by male and female, (2) to male-only care (4). Although this scoring system does not quantify absolute
parental effort, it quantifies relative participation of sexes, which is the metric we were interested in here.
Scores were gathered separately for nest building, incubation, nest guarding (i.e., guarding and defending
the nest during incubation), chick brooding, chick feeding, chick guarding (i.e., guarding and defending the
brood after hatching), post-fledging feeding of chicks, and post-fledging guarding of chicks (i.e., guarding
and defending the brood after fledging, for details see (1)). Scoring was a necessity rather than preference,
since quantitative data were not available for many species. This is a common practice in comparative
studies; see (2–6) for similar approaches. Our scoring was significantly repeatable (sensu (7)) between
two independent observers who scored a subset of species (intraclass correlation, repeatability of mean
score of all care components: rICC = 0.79, F = 8.6, p < 0.001, n = 31 species). These scores also correlate with
an independent measure of care (i.e., sex differences in the length of care, see (8)). Data collection was
designed to cover the broad phylogenetic diversity and full variability of breeding systems exhibited by
birds. Our data set contained 659 species from 113 avian families. Sample size differed between individual
analyses, because not all traits were available for all species (see below). There were too many missing
values in some of the parental activities to allow data enhancement by imputation.
To represent the extent of biparental care, the eight parental activities were re-coded on a 3 level scale so
that 0 represented exclusive uniparental care by the male or female (original scores 0 or 4), 1 represented
were available for all species (average number of activities = 4.83, SD = 1.56, n = 659 species; all activities
were available only for 28 species). At the same time, means for different parental activities ranged from
0.58 for incubation to 1.69 for post-fledging feeding across species. Consequently, differences between
activity-specific means could have introduced bias into the calculation of parental cooperation for every
species depending on which activity happened to lack for a particular species. Therefore, before averaging
across activities we centered the extent of biparental care for each activity by subtracting the mean from
the original score. The resulting parental cooperation ranged from minimum parental cooperation to
maximum parental cooperation (frequency distribution of parental cooperation across 659 species of
birds is available in Fig. S1) and varied across the phylogeny (Fig. 1). Here, minimum cooperation is when
all activities are carried out by one sex (the male or the female, ca. around the value of −1.5), whereas the
maximum cooperation is when all parental care activities are shared approximately equally between the
male and the female (ca. around the value of 1.5). To test specific hypotheses that predict effects on the
scale from female-biased to male-biased care, we calculated in the same way as above centered values of
the original scores of sex-specific engagement in parental care. Resulting values of this relative male care
ranged from −2 (strongly female-biased care) to 3 (strongly male-biased care; frequency distribution of
relative male care across 659 species of birds is available in Fig. S1). Note that for sake of simplifying the
analyses, we worked with the ordinal scores as if they were continuous variables (for the necessity to
work with ordinal scores see above).
We used two proxies of sexual selection that are widely available: sexual size dimorphism and extra-pair
paternity (9). We calculated size dimorphism index as SDI = body mass of the heavier sex divided by body
mass of the lighter sex minus one and made the values positive for male-biased dimorphism and negative
for female-biased dimorphism. We then also calculated absolute SDI by taking absolute values of the
original SDI. Greater value of the absolute SDI thus means greater difference in body masses between
sexes, suggesting differential selection acting on males and females that may indicate sexual selection (10,
11). Indeed, when we quantified percentage of polygamous pairings of males and females and calculated
absolute difference between the sexes, this difference correlated positively with absolute SDI (r = 0.28, n =
496 species). This showed that extensive sexual size dimorphism was correlated with divergent mating
strategies of the two sexes indicating strong sexual selection. Extra-pair paternity was expressed as % of
broods containing at least one extra-pair offspring (EPP), in accordance with recent studies (12). However,
to check the sensitivity of our analyses to this particular choice, we also repeated all analyses with % of
extra-pair offspring in the population (EPY). Although this variable dramatically decreased sample size,
results were robust to the choice of EPP vs. EPY (details of these sensitivity analyses are available in Tables
Social environment was characterized by adult sex ratio (ASR), which was expressed as the proportion of males in the adult population (13, 14). We then calculated the absolute deviation from ASR of 0.5 to express the degree of bias in the frequency of males vs. females in the population. This value was always positive and increased with increasing deviation from ASR of 0.5 (ASR bias).
To characterize ambient environment, first we recorded breeding season for each species from literature. Second, based on digitized ranges (15) and global climatic layers (CRU Dataset,
http://www.cru.uea.ac.uk/), we extracted climatic conditions in the breeding range of every species during its breeding season. We extracted i) the average monthly temperature (∘C) and rainfall (mm); ii)
within-year variation as SD of breeding season monthly averages for temperature and rainfall; and iii) among-year variation as SD across 49 years (1961-2009) of monthly averages for temperature and rainfall during the species' breeding season. Rainfall was log-transformed prior to all calculations. We excluded seabirds from all the analyses, as climatic variables do not affect their food supply in the same way as in terrestrial birds (Procellariiformes, Sphenisciformes, Alcidae, Fregatidae, Sulidae, Pelecanidae, some Sternidae, Laridae, Stercorariidae, and Phalacrocoracidae).
To control for potential confounds, we included the following life-history traits in the models. For every species in our dataset, we obtained estimates of body mass of males and females (g) and used their average, and chick development (altricial vs. precocial). Body mass captures many aspects of species’ life history, including adult mortality (16), and thus pair bond duration and divorce rate (17, 18). Demanding chicks (i.e. altricial) preclude the evolution of reduced parental care (19–21). In a previous study of shorebirds, species with less demanding (i.e. precocial) young exhibited uniparental care with higher probability than species with more demanding (i.e. semiprecocial) young (20). Thus, chick development could influence parental cooperation by setting overall offspring demand. Since the length of breeding cycle might influence parental cooperation (22), we also recorded durations of breeding cycle phases (nest building, incubation, chick feeding, post-fledging care). However, we were able to find durations of all four phases only for 214 out of our 659 species. All these durations correlated well with body mass (for the relationship of breeding cycle duration to adult body mass in our dataset see Fig. S4) and thus to avoid decreasing the sample size, we modeled only adult body mass.
Phylogenetic analyses
We used phylogenetic generalized least squares (PGLS) approach implemented in a fast likelihood
parameter estimates. In Table 1 in the main text, we present average values of parameters and test
statistics, whereas in this Supporting Information we also present their 95% CIs. The non-random
distribution of species ranges across the globe could potentially introduce spatial autocorrelation,
therefore we checked for spatial autocorrelations in residuals from our models by i) fitting
semi-variograms and ii) estimating Moran’s I based on the latitude and longitude of the centroid of each species’
range. Indeed, there was no indication of significant spatial autocorrelation in residuals from our models
(Fig. S5).
Parental cooperation and relative male care were the main response variable in our models. First, we
fitted bivariate PGLS models between parental cooperation and the following predictors: sexual size
dimorphism (log absolute SDI), extra-pair paternity (sqrt EPP), adult sex ratio (sqrt ASR bias), climatic
variables (means and among- and within-year variations in temperature and rainfall), adult body mass
(log-transformed), and chick development (altricial vs precocial). Predictors were the same for relative
male care, except that we used SDI instead of absolute SDI, ASR instead of ASR bias, and we did not use
climatic variables due to lacking predictions for relative male care. Second, we fitted PGLS models with
several explanatory variables. To reduce the number of predictors in these multiple regression models, we
performed a Principal Components Analysis on all six climatic variables and extracted the first two PCs,
which represented temperature (PC.temperature: higher values mean hot environments with low
temperature variability) and rainfall (PC.rainfall: higher values mean dry environments with high rainfall
variability), respectively (Table S4). These two axes explained 76.4% of variation in climatic variables. We
used these PCs as predictors in multiple PGLS regression models to reduce multicollinearity of predictors.
To use the maximum number of species in each analysis, we fitted four models structured according to our
three main hypotheses while controlling for life-history variables. For parental cooperation, these were:
Sexual selection model – absolute SDI, EPP, adult body mass, chick development (n = 226 species); Social
environment model – ASR bias, adult body mass, chick development (n = 165 species); Climate model –
PC.temperature, PC.rainfall, adult body mass, chick development (n = 659 species); Full model – absolute
SDI, EPP, ASR bias, PC.temperature, PC.rainfall, adult body mass, chick development (n = 80 species). For
relative male care, these were: Sexual selection model – SDI, EPP, adult body mass, chick development (n =
226 species); Social environment model –ASR, adult body mass, chick development (n = 165 species); Full
model – SDI, EPP, ASR, adult body mass, chick development (n = 80 species). We did not fit the climatic
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Fig.%S1.!Frequency!distribution!of!parental!cooperation!and!relative!male!care!in!birds!(n!=!659!species).!
Parental!cooperation!varies!between!1.5!when!the!male!and!the!female!parent!share!care!provisioning!
approximately!equally!and!−1.5!when!only!one!parent!(the!male!or!the!female)!provides!all!care,!with!most!
species!clustered!around!0!when!the!share!of!the!two!sexes!is!roughly!2:1.!Relative!male!care!varies!from!
strongly!femaleIbiased!(ca.!−2)!to!strongly!maleIbiased!(ca.!3).!The!bottom!panel!shows!graphically!how!
relative!male!care!was!recoded!to!express!parental!cooperation.!Note!that!the!scales!of!both!parental!
cooperation!and!relative!male!care!are!arbitrary!and!based!on!our!system!of!scoring!(Supplement!S1).!
Parental cooperation
N
o
.
o
f
sp
e
ci
e
s
More biparental care More uniparental care
1.5 1.0 0.5 0.0 0.5 1.0 1.5
0
2
0
4
0
6
0
8
0
Relative male care
N
o
.
o
f
sp
e
ci
e
s
2 1 0 1 2 3
0
5
0
1
0
0
1
5
0
1.0 0.5 0.0 0.5 1.0
1
0
1
2
Parental cooperation
R
e
la
ti
v
e
ma
le
ca
re
Fig.%S2.!Parental!cooperation!in!relation!to!predictors!(see!Table!1):!sexual!size!dimorphism!(log10I
transformed!absolute!Sexual!Dimorphism!Index),!extraIpair!paternity!(squareIroot!transformed!EPP),!adult!
sex!ratio!(squareIroot!transformed!ASR!bias),!ambient!temperature!(PC1!from!PCA!on!climatic!variables,!
factor!loadings!available!in!Table!S4),!rainfall!(PC2!from!PCA!on!climatic!variables,!factor!loadings!available!in!
Table!S4),!body!mass!(log10Itransformed!adult!body!mass),!and!chick!development!(categorical!variable!coded!
as!altricial!vs.!precocial).!Raw!data!and!a!lowess!smoother!line!are!depicted.!
−4 −3 −2 −1 0
− 1 .0 0 .0 1 .0
Sexual size dimorphism
P a re n ta l co o p e ra ti o n
0 2 4 6 8 10
− 1 .0 0 .0 1 .0
Extra−pair paternity
P a re n ta l co o p e ra ti o n
0.0 0.1 0.2 0.3 0.4 0.5
− 1 .0 0 .0 1 .0
Adult sex ratio
P a re n ta l co o p e ra ti o n
−0.6 −0.2 0.2 0.4
− 1 .0 0 .0 1 .0 Ambient temperature P a re n ta l co o p e ra ti o n
−0.4 0.0 0.2 0.4
− 1 .0 0 .0 1 .0 Rainfall P a re n ta l co o p e ra ti o n
2 4 6 8 10 12
Fig.%S3.!Relative!male!care!in!relation!to!predictors!(see!Table!S2):!sexual!size!dimorphism!(Sexual!
Dimorphism!Index),!extraIpair!paternity!(squareIroot!transformed!EPP),!adult!sex!ratio!(ASR),!body!mass!
(log10I!transformed!adult!body!mass),!and!chick!development!(categorical!variable!coded!as!altricial!vs.!
precocial).!Raw!data!and!a!lowess!smoother!line!are!depicted.!An!extreme!value!of!Sexual!Dimorphism!Index!=!
2.14!(Great!Bustard!Otis%tarda)!is!excluded!from!the!first!panel.!
!
−1.0 0.0 0.5 1.0
−
1
0
1
2
Sexual size dimorphism
R e la ti ve ma le ca re
0 2 4 6 8 10
−
1
0
1
2
Extra−pair paternity
R e la ti ve ma le ca re
0.3 0.4 0.5 0.6 0.7
−
1
0
1
2
Adult sex ratio
R e la ti ve ma le ca re
2 4 6 8 10 12
